Context‐dependent use of muscle spindles for human position sense

To stand, walk, reach and grasp, we use internal representations of our body position. Among the contributors to our position sense are the muscle spindles. In 1972, Goodwin and colleagues established that these mechanoreceptors have a profound role for indicating body orientation. Muscle spindles are now regarded as the dominant source of body positional information encoding static and dynamic cues of muscle length (Proske & Gandevia, 2012), thus providing information referenced to the body. Position sense, however, can also originate from externally referenced signals, such as vision, that depict where our body is located with respect to the environment. Our brain is consistently challenged to integrate and consolidate body- and externally-referenced sensory information for spatial representations used in perception and the control of movement (Paillard 1991). Are all sensory signals used in a universal manner for position sense? In particular, muscle spindle cues are crucial for perceiving inter-limb orientation, but are such inputs relied upon to determine a limb's position in external space? In this issue of The Journal of Physiology, Tsay and colleagues (2016) address this question by biasing the muscle spindle signals during an elbow joint localization task. The authors demonstrate that the use of muscle spindle cues for limb localization is context dependent. The localization task utilized by Tsay et al. (2016) involved obstructing one arm from view and passively moving it to a position of elbow flexion or extension (the reference arm). Participants were required to spatially localize and indicate its perceived position in two ways: (1) by aligning its perceived position with the contralateral arm (limb matching task) and (2) by adjusting an external device to the perceived arm position (pointing task). The important difference between these two tasks is the available sensory cues which can be used for joint localization. During limb matching, the brain can compare sensory signals from both arms, whereas the pointing task involves using signals from the reference arm to indicate its position in external space. To evaluate muscle spindle contributions to these position sense tasks, the authors conditioned elbow muscles with isometric contractions to 'set' muscle spindles to a desired state and vibrated elbow muscles to increase spindle afferent discharge. Through these experimental manipulations, Tsay et al. (2016) reveal that muscle spindle signals influence the performance of elbow joint localization during limb matching, but not in pointing. These results may come as a surprise but, as the authors propose, they are a likely reflection of the context in which limb position is perceived. The authors suggest that during limb matching, the perceived limb position relies on the orientation of body segments with respect to each other. A comparison of body-referenced muscle spindle signals between arms is not only relevant, but useful for the limb matching performance. This fits with previous findings of inter-limb matching (Proske & Gandevia, 2012) and supports the hypothesis that the brain relies on the difference of sensory signals between limbs during such localization tasks (Tsay et al. 2014). Conversely, pointing involves identifying the spatial coordinates of a limb in external space. The external pointer device is visually guided for the localization task and a difference of limb-referenced cues does not aid in representing this orientation. The possible use of sensory signals is therefore determined by whether the context of position sense concerns the body alone or the body in external space, fitting with previous models of sensorimotor control (Paillard 1991). The findings of Tsay and colleagues represent a significant addition to our understanding of human position sense. Muscle spindles are confirmed to be a primary source of positional information, but mainly to estimate body-referenced orientation of the limbs. Consequently, their findings establish that, although human positional sense is based on the integration of cues from multiple sources, the relative contribution of sensory signals to positional sense is task dependent. These findings lay the foundation for future studies but also computational models to reveal the neural principles underlying human positional sense. Such a context-dependent use of spindle information for position sense could stem from learning: under normal circumstances, estimating the state of one limb with respect to another can be derived from a simple (approximate) solution comparing spindle information from both limbs. On the other hand, such approximation is not possible when the state of a limb is estimated with respect to the environment. In this latter scenario, state estimation of the target limb must be performed through fusion of available sensory signals, probably ignoring the bias in spindle information induced by Tsay et al. (2016). Further, we may speculate regarding the potential implications of the findings by Tsay and colleagues to sensorimotor processes outside of perception. Many sensory transformations require the use and integration of limb or whole-body positional information to function. Whether the context of the sensory transformation requires a body-referenced or an externally referenced representation of limb, trunk or head position may influence the relative importance of muscle spindle information in the transformation process. Similarly, sensory contributions to motoneuronal drive during movement may be affected by the context in which movements are performed. Based on the findings reported in the focus paper, it is tempting to propose that motoneuronal drive to the elbow flexors and extensors during matching bilateral elbow movements may involve greater relative contribution from muscle spindles than similar movements performed under visual guidance. These as well as other potential implications highlight the novelty and importance of the findings by Tsay et al. (2016). No competing interests declared.

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